Frequency-dependent fitness in gynodioecious<i>Lobelia siphilitica</i>

Rivkin, L. Ruth; Case, Andrea L.; Caruso, Christina M.

doi:10.1111/evo.12654

Cited by 12 publications

(9 citation statements)

References 70 publications

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“…; Rivkin et al. ), this is the first example of a frequency‐dependent trait driving differential exposure to natural enemies. Moreover, we would predict stronger frequency dependence in disease exposure than pollen limitation in this system, because it is the rate of pollination rather than the eventual outcome that drives closing response.…”

Section: Discussionmentioning

confidence: 94%

“…Female flowers closed rapidly in arrays where they were rare, and stayed open longer in arrays where they were common. Although negative frequency-dependent selection for females is predicted (Maurice and Fleming 1995;McCauley and Taylor 1997) and has been empirically demonstrated in the context of pollen limitation (McCauley and Brock 1998;De Cauwer et al 2010;Rivkin et al 2015), this is the first example of a frequency-dependent trait driving differential exposure to natural enemies. Moreover, we would predict stronger frequency dependence in disease exposure than pollen limitation in this system, because it is the rate of pollination rather than the eventual outcome that drives closing response.…”

Section: Floral Traits Affecting Disease Exposurementioning

confidence: 91%

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The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

et al. 2018

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In flowering plants, the evolution of females is widely hypothesized to be the first step in the evolutionary pathway to separate male and female sexes, or dioecy. Natural enemies have the potential to drive this evolution if they preferentially attack hermaphrodites over females. We studied sex-based differences in exposure to anther-smut (Microbotryum), a sterilizing pollinator-transmitted disease, in Dianthus pavonius, a gynodioecious perennial herb. We found that within a heavily diseased population, females consistently had lower levels of Microbotryum spore deposition relative to hermaphrodites and that this difference was driven by rapid floral closing in females following successful pollination. We further show that this protective closing behavior is frequency-dependent; females close faster when they are rare. These results indicate that anther-smut disease is an important source of selection for females, especially since we found in a common garden experiment no evidence that females have any inherent fecundity advantages over hermaphrodites. Finally, we show that among populations, those where anther-smut is present have a significantly higher frequency of females than those where the disease is absent. Taken together our results indicate that anther-smut disease is likely an important biotic factor driving the evolution and maintenance of females in this gynodioecious species.

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Section: Discussionmentioning

confidence: 94%

Section: Floral Traits Affecting Disease Exposurementioning

confidence: 91%

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

et al. 2018

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“…Although present in only 5‐6% of angiosperm species (Renner and Ricklefs, ; Charlesworth, ), the evolution of separate sexes is a recurring transition in angiosperms (Geber et al., ; Charlesworth, ; Renner, ). The occurrence of two mating types in populations, for example, females and males in dioecious populations or females and hermaphrodites in gynodioecious populations, has direct effects on patterns of mating as well as important emergent consequences such as the evolution of sexual dimorphism (Barrett and Hough, ; Kamath et al., ) and sex ratio evolution (McCauley and Taylor, ; Van Etten and Chang, ; Rivkin et al., ). A common pathway to separate sexes is the origin and spread of male‐sterility in otherwise hermaphroditic populations (i.e., gynodioecy; Webb, ; Spigler and Ashman, ).…”

mentioning

confidence: 99%

Colonization, Baker's law, and the evolution of gynodioecy in Hawaii: implications from a study of Lycium carolinianum

Miller

Blank

Levin

2019

American J of Botany

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Premise As Baker’s law suggests, the successful colonization of oceanic islands is often associated with uniparental reproduction (self‐fertility), but the high incidence of dimorphism (dioecy, gynodioecy) on islands complicates this idea. Lycium carolinianum is widespread, occurring on the North American mainland and the Hawaiian Islands. We examined Baker's ideas for mainland and island populations of L. carolinianum and examined inbreeding depression as a possible contributor to the evolution of gynodioecy on Maui. Methods Controlled crosses were conducted in two mainland populations and two populations in Hawaii. Treatments included self and cross pollination, unmanipulated controls, and autogamy/agamospermy. Alleles from the self‐incompatibility S‐RNase gene were isolated and compared between mainland and island populations. Given self‐compatibility in Hawaii, we germinated seeds from self‐ and cross‐ treatments and estimated inbreeding depression using seven traits and a measure of cumulative fitness. Results Mainland populations of Lycium carolinianum are predominately self‐incompatible with some polymorphism for self‐fertility, whereas Hawaiian populations are self‐compatible. Concordantly, S‐RNase allelic diversity is reduced in Hawaii compared to the mainland. Hawaiian populations also exhibit significant inbreeding depression. Conclusions Self‐compatibility in Hawaii and individual variation in self‐fertility in mainland populations suggests that a colonization filter promoting uniparental reproduction may be acting in this system. Comparison of S‐RNase variation suggests a collapse of allelic diversity and heterozygosity at the S‐RNase locus in Hawaii, which likely contributed to mate limitation upon arrival to the Pacific. Inbreeding depression coupled with autonomous self‐fertilization may have led to the evolution of gynodioecy on Maui.

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“…The importance of spatial scale may be more severe in plants than in animals because the ability of plants to respond to selective interference through behavioral modification is likely limited to shifts in phenology (e.g., Rivkin et al. ; Weis et al. ).…”

Section: Introductionmentioning

confidence: 99%

“…As the scale of interaction reduces, as expected under local competition with neighboring individuals or short range movements of pollinators, we expect greater opportunity to arise as individual plants experience variable contexts. The importance of spatial scale may be more severe in plants than in animals because the ability of plants to respond to selective interference through behavioral modification is likely limited to shifts in phenology (e.g., Rivkin et al 2015;Weis et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Scale dependence of sex ratio in wild plant populations: implications for social selection

Sanderson

Augat

Taylor

et al. 2016

Ecology and Evolution

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Social context refers to the composition of an individual's social interactants, including potential mates. In spatially structured populations, social context can vary among individuals within populations, generating the opportunity for social selection to drive differences in fitness functions among individuals at a fine spatial scale. In sexually polymorphic plants, the local sex ratio varies at a fine scale and thus has the potential to generate this opportunity. We measured the spatial distribution of two wild populations of the gynodioecious plant Silene vulgaris and show that there is fine‐scale heterogeneity in the local distribution of the sexes within these populations. We demonstrate that the largest variance in sex ratio is among nearest neighbors. This variance is greatly reduced as the spatial scale of social interactions increases. These patterns suggest the sex of neighbors has the potential to generate fine‐scale differences in selection differentials among individuals. One of the most important determinants of social interactions in plants is the behavior of pollinators. These results suggest that the potential for selection arising from sex ratio will be greatest when pollen is shared among nearest neighbors. Future studies incorporating the movement of pollinators may reveal whether and how this fine‐scale variance in sex ratio affects the fitness of individuals in these populations.

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Frequency-dependent fitness in gynodioeciousLobelia siphilitica

Cited by 12 publications

References 70 publications

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

Colonization, Baker's law, and the evolution of gynodioecy in Hawaii: implications from a study of Lycium carolinianum

Scale dependence of sex ratio in wild plant populations: implications for social selection

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